Adaptation to environmental stress by evolution of non-genotypic heterogeneity within microbial populations

Lead Research Organisation: University of Nottingham
Department Name: School of Life Sciences

Abstract

In order to survive in the natural environment, microorganisms must be able to cope with stresses arising from environmental change and perturbation. Sources of environmental stress include natural environmental pressures stemming from climate fluctuations and occasional exposure to harmful elements. In addition, pollution arising from human activities releases potentially-toxic contaminants. It is generally accepted that one key factor which helps species to survive such environmental stresses is the presence of 'genetic variation' within populations, arising from differences in DNA sequence among individual organisms of the same species. This variation means that individuals will have some slightly different characteristics, making it likely that some of the population will be better adapted to withstand particular stressful conditions and allow the species to survive. While such genetic variation is clearly very important, scientific advances over recent years have indicated that there is an additional factor important for the survival of environmental stresses. Experiments with single-cell microorganisms have shown that individual cells within a population have markedly different abilities to survive environmental stresses, despite having the same DNA composition (i.e. being genetically-uniform). This discovery has suggested that this new source of variation, known as 'non-genotypic heterogeneity', may be a major factor allowing microorganisms to survive and overcome environmental stress in nature. However, nearly all of the research into this topic has so far been performed only under model conditions with laboratory organisms. Our recent NERC-funded work has been the first to examine the importance of non-genotypic heterogeneity for microorganisms living in the natural environment, with extremely promising results.

Our studies to date have indicated that wild yeasts with high levels of non-genotypic heterogeneity have a competitive advantage over yeasts with lower heterogeneity in polluted habitats. Furthermore, these yeasts evolve the property of increased non-genotypic heterogeneity over time when subject to environmental stress. These important breakthroughs for microbial ecology underpin our new proposal. The objective now is to describe the wider importance of these exciting findings and, for the first time in wild cell populations selected by environmental stress, to uncover the mechanisms that underlie increased non-genotypic heterogeneity. We have three particular aims, as follows. (1) To determine how applicable our findings-to-date are more broadly. This will involve testing non-genotypic heterogeneity at environmental sites subject to quite diverse selection pressures as well as interrogation of a wide range of organisms, including bacteria. (2) To characterise the changes in DNA sequence that allow organisms to adapt to environmental stress by evolving increased non-genotypic heterogeneity. (3) To elucidate how these DNA sequence changes cause increased heterogeneity. We will adopt cutting-edge new techniques to achieve these objectives. The work could also have important applications, for example through the development of heterogeneity "markers" as novel biological reporters of pollutants in the natural environment. The results of the proposed project are anticipated to provide major new insights into non-genotypic heterogeneity as a survival strategy for species during environmental change. This will help greatly in our understanding of how microorganisms persist in the natural environment, and how they may react to harmful changes caused by humans through pollution.

Planned Impact

Who will benefit from this research?

The principal economic and societal beneficiaries will be all those who gain from improved understanding of microbial diversity and survival in the natural environment; principally, the following: (1) Regulatory bodies concerned with environmental change and pollution. (2) Organizations providing environmental monitoring services. (3) Parties concerned with sustaining biodiversity in the environment. (4) The brewing, baking and other industries that exploit yeasts. (5) The general public. (6) Researchers and collaborators who are directly involved in the project.

How will they benefit from this research?

(1) With the increasing prominence of environmental issues for policy makers at government and inter-government levels, the improved understanding of impacts on organisms in the wild that this project will bring will help to guide the development of future policies on environmental change and pollution. As microorganisms are at the base of the food chain, new understanding of their responses to toxic pollutants also improves understanding of potential impacts on health of higher organisms including humans.

(2) It is anticipated that this project will reveal novel genetic markers of non-genotypic heterogeneity, with potential for application as innovative diagnostic probes of ecosystem health. Such assays have commercial value, and could be developed during the one to two years immediately following completion of the project.

(3) Biodiversity is a major scientific theme of the NERC and this project will fill a major gap in our understanding of biodiversity - the importance of non-genotypic heterogeneity for the survival of wild species during environmental change. Furthermore, this project will generate a library of wild microbial isolates all characterised for non-genotypic heterogeneity (diversity), from defined polluted and non-polluted locations across the UK. This will be a unique and valuable resource available to the broader community.

(4) The economic efficiency of industries like brewing and baking hinges strongly on optimal performance of the yeast that they use. Non-genotypic heterogeneity impacts this as only a subpopulation of cells may be performing optimally at any time. Although this proposal focuses on heterogeneity in the context of environmental stress, knowledge generated here could be exploited to help improve the efficiency of industrial operations with yeasts and so promote wealth generation.

(5) The proposed research is in an area that we have found appeals to the interests of the general public, from presentations we have given at University open days and outreach activities. Moreover, new awareness from this project will help to inform the public debate that contributes to environmental policy development.

(6) Staff working on this project will gain valuable new research skills as well as transferable skills like oral and written communication, collaboration, networking, and working as part of a team. The PDRA will receive specific exposure to science-to-policy initiatives and in communicating science to the public. These skills will improve their employment prospects in all sectors and their contribution to the economic competitiveness of the United Kingdom.
 
Description We have shown that selection for increased heterogeneity is not a ubiquitous feature of all polluted environments. It may not apply to more static environments, and population-averaged resistance may be more strongly selected than resistance-heterogeneity in some situations. We have preliminary evidence that high-heterogeneity isolates may have cross-pollutant heterogeneity (e.g. in Cu and Pb resistance). We have shown through experimental evolution that heterogeneity (in Cu resistance) evolves in Cu-supplemented batch cultures of yeast. we have shown that ploidy of natural yeast isolates is related to heterogeneity. We are developing a new method for assessing hypha-hypha heterogeneity in filamentous fungi, according to individual-hypha growth rates. We are obtaining and analysing genome-sequence data for yeast isolates that may give insights to mechanisms by which heterogeneity evolves in stressed environments.
Exploitation Route Changes to environmental monitoring practices
Sectors Agriculture, Food and Drink,Environment

 
Description Undergraduate Summer Bursary, 2015
Amount £1,850 (GBP)
Organisation British Mycological Society 
Sector Learned Society
Country United Kingdom
Start 06/2015 
End 08/2015
 
Description Conference organiser 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Conference organiser, British Mycological Society Main Meeting
Year(s) Of Engagement Activity 2017
 
Description Pollutants and Biodiversity Workshop, at UP campus Nottingham 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other audiences
Results and Impact Workshop I organised, attracting 30 delegates from academia and industry
Year(s) Of Engagement Activity 2016